most birds have only left ovary but 2 ovaries are typical of many raptors

contains from 500 to several thousand primary oocytes

Testes & follicles increase dramatically in size as the breeding season
approaches.

As day length increases, photic stimulation of the hypothalamus results
in the secretion of Gonadotropin releasing hormone (GnRH below). When activated
by GnRH, the anterior pituitary secretes two gonadotropin hormones, follicle-stimulating
hormone (FSH) and luteinizing hormone (LH). FSH acts on sperm-producing
structures in the testes, while LH acts on the interstitial cells of the testes
causing them to secrete the steroid hormone testosterone. The pituitary
gland monitors the amount of testosterone in the blood, thus creating a
negative feedback loop to maintain hormone levels within a set range (Akins
and Burns 2001).

Ambient visual cues, such as daylight, activate photosensitive loci in
the brain both indirectly, through the eyes, and directly, through the
skull. The hypothalamus of the bird brain contains special cells that are
sensitive to extremely low light levels, intensities comparable to the
amount of light that can penetrate brain tissue (Akins and Burns 2001).

From: Akins and Burns (2001)

The pattern of testosterone secretion in free-living populations of Song Sparrows.
Plasma levels peak in April and May as breeding got underway and then were maintained at a lower “breeding baseline” during the
rest of the breeding season. As prebasic molt ensued, plasma levels of testosterone were basal and remained so throughout autumn and winter.
From: Wingfield and Hahn (1994).

Biological actions of the steroid hormone testosterone. The morphological, physiological and behavioral actions of testosterone that are essential
for male reproductive function are given on the right hand and lower sides of the figure. The “costs” of prolonged high levels of testosterone are given on the
left hand side in italics. The patterns of plasma testosterone levels may be a function of secretion patterns to maintain male reproductive function, and “costs”
of testosterone that require that plasma levels be low. From Wingfield et al. (2000).

Testosterone increases availability of carotenoids -- Androgens and carotenoids play a fundamental role in the expression of secondary sex traits in animals that communicate information on individual quality. In birds, androgens regulate song, aggression, and a variety of sexual ornaments and displays, whereas carotenoids are responsible for the red, yellow, and orange colors of the integument. Parallel, but independent, research lines suggest that the evolutionary stability of each signaling system stems from tradeoffs with immune function: androgens can be immunosuppressive, and carotenoids diverted to coloration prevent their use as immunostimulants. Despite strong similarities in the patterns of sex, age and seasonal variation, social function, and proximate control, there has been little success at integrating potential links between the two signaling systems. These parallel patterns led us to hypothesize that testosterone increases the bioavailability of circulating carotenoids. To test this hypothesis, Blas et al. (2006) manipulated testosterone levels of Red-legged Partridges (Alectoris rufa) while monitoring carotenoids, color, and immune function. Testosterone treatment increased the concentration of carotenoids in plasma and liver by >20%. Plasma carotenoids were in turn responsible for individual differences in coloration and immune response. These results provide experimental evidence for a link between testosterone levels and immunoenhancing carotenoids that (i) reconciles conflicting evidence for the immunosuppressive nature of androgens, (ii) provides physiological grounds for a connection between two of the main signaling systems in animals, (iii) explains how these signaling systems can be evolutionary stable and honest, and (iv) may explain the high prevalence of sexual dimorphism in carotenoid-based coloration in animals.

Red-legged Partridge (Photo by G. Bortolotti)

Sperm production

occurs in seminiferous tubules of the testes (shown below)

occurs best at slightly cooler temperatures, so spermatogenesis may occur
primarily at night when body temperatures are slightly lower

sperm are stored at the terminal end of the vas deferens (seminal glomus),
and this creates a swelling called the cloacal protuberance

Male birds have paired abdominal testes lying cranioventral
to the first kidney lobe. Testes increase dramatically in size during the
breeding season. The vas deferens emerges medially and passes caudally
to the cloaca where it has a common opening with the ureter in the Urodeum.
The terminal vas deferens is swollen as a storage organ: the seminal glomus
(or seminal vesicle as in the drawing to the right).

As in mammals, sperm formation is temperature sensitive,
and maturation is assisted by nocturnal drops in temperature, or by the
development of scrotal-like external thermoregulatory swellings holding
the seminal glomera.

In addition, male birds tend to have relatively low extragonadal
sperm reserves and sperm are ejaculated soon after production in the testes.

Sperm competition and testes size -- Comparative analyses suggest that a variety of ecological and behavioural factors contribute to the
tremendous variability in extrapair mating among birds. In an analysis of 1010 species of birds, Pitcher et al. (2005) examined several ecological
and behavioural factors in relation to testes size; an index of sperm competition and the extent of extrapair mating. In univariate and multivariate
analyses, testes size was significantly larger in species that breed colonially than in species that breed solitarily, suggesting that higher breeding
density is associated with greater sperm competition. After controlling for phylogenetic effects and other ecological variables, testes size was also
larger in taxa that did not participate in feeding their offspring. In analyses of both the raw species data and phylogenetically independent contrasts,
monogamous taxa had smaller testes than taxa with multiple social mates, and testes size tended to increase with clutch size, which suggests that
sperm depletion may play a role in the evolution of testes size. These results suggest that traditional ecological and behavioural variables, such as
social mating system, breeding density and male parental care can account for a significant portion of the variation in sperm competition in birds.

Testis size increases with colony size in Cliff Swallows
-- By using a sample of over 800 male Cliff Swallows (Petrochelidon
pyrrhonota) that died during a rare climatic event in their Nebraska
study area in 1996, Brown and Brown (2003) investigated how testis size
was related to body size, age, parasite load, and a bird's past colony-size
history. Testis volume increased with body size. After correcting for body
size, testis volume was lowest for birds age 1 and 2 years but did not
vary with age for males 3 years old or more. Birds occupying parasite-free
(fumigated) colonies had significantly larger testes than did birds at
nonfumigated sites. Testis volume increased significantly with the size
of the breeding colonies a bird had used in the past. These results show
within a species that larger testes are favored in more social environments,
probably reflecting a response to increased rates of extrapair copulation
(and thus sperm competition) among Cliff Swallows in large colonies. The
presence of ectoparasites, by inflating levels of plasma corticosterone,
may in turn reduce testis mass. These data provide no support for the hypothesis
that large testes, perhaps by producing more testosterone, are immunosuppressive
and thus costly for that reason.

Temperature and the timing of reproduction -- Many bird species reproduce earlier in years with high spring temperatures, but little is known about the causal effect of temperature. Temperature may have a direct effect on timing of reproduction, but the correlation may also be indirect, for instance via food phenology. As climate change has led to substantial shifts in timing, it is essential to understand this causal relationship to predict future impacts of climate change. Visser et al. (2009) tested the direct effect of temperature on laying dates in Great Tits (Parus major) using climatized aviaries in a 6-year experiment. Temperature patterns from two specific years in which the wild population laid either early (‘warm’ treatment) or late (‘cold’ treatment) were mimicked. Laying dates were affected by temperature directly. Because the relevant temperature period started three weeks prior to the mean laying date, with a range of just 4°C between the warm and the cold treatments, and because the birds were fed ad libitum, it is likely that temperature acted as a cue rather than lifting an energetic constraint on the onset of egg production. Visser et al. (2009) also found a high correlation between the laying dates of individuals reproducing both in aviaries and in the wild, validating investigations of reproduction of wild birds in captivity. These results demonstrate that temperature has a direct effect on timing of breeding, an important step towards assessing the implication of climate change on seasonal timing.

Egg production

Most birds have only one ovary and one oviduct. In early stages of embryonic
development, each female bird has two ovaries; only the left one develops
into a functional organ. In some birds, such as hawks, the right ovary
and oviduct usually develop. A mature ovary looks like a cluster of grapes.
and may contain up to 4,000 small ova which can develop into mature ova.

In most birds, only the left ovary and oviduct
persist. The ovary enlarges greatly during the breeding season. Active
ovaries resemble bunches of tiny grapes -- the developing follicles. The
oviduct opens medially to it in a funnel-shaped ostium. Ovulation results
in the release of an egg from a mature follicle on the surface of the ovary.
The egg, with extensive food reserves in the form of concentric layers
of yolk, is picked
up by the ostium and ciliary currents carry it into the magnum
region. Over about three hours the egg receives a coating of albumen.

The egg then passes into the isthmus,
where the shell membranes are deposited. This takes about one hour. The
egg them moves to the uterus, or shell gland, where the calcareous
shell is added and, in some birds, pigment is added in characteristic patterns.
The egg then passes into the vagina and cloaca for laying.

Variation among bird species in the relative amount of yolk in eggs and the amount of energy available to the developing embryo (kJ-g -1, or kilojoules per gram). From top to bottom, the hatchlings are an altricial Brown Creeper, a semiprecocial Least Tern, a precocial Ruddy Duck, a superprecocial Mallee Fowl (Leipoa ocellata), and a Brown Kiwi (Apteryx australis). Kiwis are ‘outliers.’ Female kiwis produce extremely large eggs for their size (with substantial amounts of yolk), but young typically remain in the nest for several days and so are best classified as semiprecocial (From: Sotherland and Rahn 1987).

Kiwi lays an egg

The left egg found inside the female oviraptorosaurian.
The
texture of the shell pieces probably resembles the original
texture
of the egg. Credit: Yen-nien Cheng

Eggs discovered inside dinosaur -- The discovery
of eggs inside a dinosaur has provided new clues about dinosaur reproductive
biology and more support for the hypothesis that birds evolved from dinosaurs.
The pair of eggs are the first found inside a dinosaur. Sato et al. (2005)
found that the dinosaur produced eggs in some ways like a crocodile and
in other ways like a bird. Crocodiles have two ovaries enabling them to
lay a clutch of eggs. Birds have a single ovary and lay only one egg at
a time. The dinosaur's egg-producing capability lay somewhere in between,
suggesting a possible link with modern birds. It had two ovaries, but produce
only one egg at a time from each ovary.
Sato et al. (2005) studied a dinosaur
from a group of dinosaurs called oviraptorosaurians. This type of dinosaur
— probably 3 - 4 meters long — is a subgroup of the theropods. The dinosaur
was excavated in China. The similar size of the eggs suggests the creature's
two oviducts each produced a single egg at the same time.

Female
birds can bias the sex of their chicks.-- Whether a bird is more
likely to lay a male or female egg depends on which sex will have the greatest
chance of doing well. Rutstein et al. (2004) adjusted the food intake of
female Zebra Finches [see photo of female (left) and male (right) Zebra
Finches below right] & found that well-fed females were more likely
to produce daughters, while less well nourished birds were more likely
to have sons. This is exactly as predicted by the fact that female offspring
need to be better nourished than males if they are to survive and grow
well. The authors noted that:
“In most animals sex ratio is close to 50:50 and extremely resistant to
change. In mammals, including humans, the sex of the baby is determined
by whether the sex chromosome in the sperm is male or female. But in birds,
it is the female’s egg rather than the male’s sperm that determines what
sex the chick will be. Thus the female has the potential to determine the
sex of her young by whether she ovulates male or female eggs. In some way,
female Zebra Finches seem to be able to exert control over whether to produce
a male or female egg depending on which of the two is most likely to be
successful. Our research tells us that they do it, and we understand why.
The big question is: how do they do it?”
In many animals, females
need to be well-nourished and in good condition if they are to breed, as
eggs are costly to produce. Bigger eggs tend to lead to bigger young that
are more likely to survive. Such ‘sex ratio adjustment’ is well documented
in certain insects, such as bees and wasps, but is less well understood
in birds and mammals.
Birds are an excellent
model to use in the study of sex ratio adjustment because, using molecular
techniques, scientists can establish the sex of each egg soon after laying.
Further, all the resources given to the developing embryo are present in
the egg at laying. Thus the size and the content of the egg are measures
of the amount of resources that the female has allocated to that egg, which
affects its subsequent survival chances.
The authors explained: “We manipulated
the diet quality of Zebra Finches to look at the effects of body condition
on female investment. We found that females were able to exert a strong
degree of control over the production of male and female eggs. When females
were fed on a low quality diet, they laid eggs that were considerably lighter
than those laid when they were fed on a high quality diet, and they also
laid far more male eggs on a low quality diet. This is the converse situation
to that described 30 years ago for mammals, but it makes sense for Zebra
Finches. Previous research has shown that under poor nutritional conditions,
female Zebra Finches grow more slowly and survive less well compared to
males. Therefore, females are producing more of the sex with the highest
survival chances under those conditions.”

Two potential mechanisms for
determination among birds. (A) the
presence of the W chromosome
triggers femaleness or (B) the
presence of two Z chromosomes confers maleness.

Avian sex determination (Ellegren 2001) -- The
molecular determinants behind sexual development in birds remain a mystery.
The process is known to be different from that in mammals, with no homolog
to the gene that confers maleness in mammals found in birds. The failure
to identify such a gene in birds is probably a reflection of the fact that,
despite the occurrence of two sexes being nearly universal throughout the
animal kingdom, the genes involved seem virtually unrelated among metazoan
phyla. These differences raise obstacles for comparative or candidate gene
approaches in studies of sexual development.
In birds, females are
the heterogametic sex, with one copy each of the Z and W sex chromosomes.
Males are homogametic (ZZ). However, it is not clear whether it is the
presence of the female-specific W chromosome that triggers female development,
or the dose of Z chromosome that confers maleness. An intriguing
additional possibility is that both Z and W matter! In marsupials, for
example, Y acts as a dominant testis determining chromosome, while the
X chromosome determines the choice between pouch and scrotum. Maybe a system
where the two sex chromosomes mediate different aspects of sex differentiation
is also used in birds.

Vertebrate sex determination systems. Phylogeny of major vertebrate clades showing the sex determining systems
found in members of the respective clade. ‘Multiple’ indicates involvement of more than one pair of chromosomes in sex determination.
TSD: temperature-dependent sex determination (From: Ezaz 2006).

Incubation temperature and avian sex ratios -- Although common in reptiles, incubation temperature has not been considered to be a factor in determining sex ratios in birds. However, Goth and Booth (2005) found that incubation temperature does affect sex ratios in megapodes, which are exceptional among birds because they use environmental heat sources for incubation. In the Australian Brush-turkey(Alectura lathami), a mound-building megapode, more males hatch at low incubation temperatures and more females hatch at high temperatures, whereas the proportion is 1:1 at the average temperature found in natural mounds. Chicks from lower temperatures weigh less, which probably affects offspring survival, but are not smaller. Megapodes possess heteromorphic sex chromosomes like other birds, which eliminates temperature-dependent sex determination, as described for reptiles, as the mechanism behind the skewed sex ratios at high and low temperatures. Instead, Goth and Booth (2005) suggest a sex -biased temperature-sensitive embryo mortality because mortality was greater at the lower and higher temperatures, and minimal at the middle temperature where the sex ratio was 1:1.

Copulation & fertilization:

For most birds, copulation involves a 'cloacal kiss', with the male on
the female's back & twisting his tail under the female's

copulation typically lasts just a few seconds (but there are exceptions - see Phony phallus puts sperm ahead in bird first below)

Bald Eagles mating

White-throated Kingfishers mating

Phony
phallus puts sperm ahead in bird first-- "These birds would
be at it for 10-20 minutes," said co-author Tim Birkhead of the Red-billed
Buffalo Weaver. Males use their organ to rub females and improve their
sperm's chance of success. Few male birds have a phallus; most achieve
fertilization via a cloacal kiss. So 19th-century reports of a mock member
in the Buffalo Weaver sent Winterbotton et al. (2001) to Namibia. Catching
the birds in the act was tough, recounts Birkhead: "In 3 years we saw eight
matings." Pairs occasionally emerged from nests and flew to a nearby tree.
"I'd run after them, sweating profusely with my binoculars steaming up,"
he says. The pair would start bouncing up and down - over numerous consecutive
bouts. Compared to the 1-2 second tryst of most birds, their staying power
is unique. Yet, entry of the elusive organ was hard to make out. Even in
captivity "they performed beautifully," but the view was blocked, says
Birkhead. So they glued a piece of cardboard to an unlucky bird's member.
This did not prevent mating, suggesting that the Buffalo Weaver organ is
actually a weapon in sperm wars. By choosing a male who rubs longest or
best, females may be selecting top-quality sperm. Paternity testing revealed
that female Buffalo Weavers sire birds from multiple males, providing evidence
of sperm competition. Time spent courting must be shown to predict sperm
transfer or success to really back up the idea. The 1.5-cm appendage lacks
blood vessels and has a twisted furrow down its length. Males in communal
nests have longer ones than those that live alone, showing that size is
a factor in social success. But for males at least, the phallus is for
more than foreplay. -- Helen
Pearson, Nature Science Update

(A) Harlequin Duck (Histrionicus histrionicus) and (B) African Goose (Anser cygnoides), two species with a short phallus and no forced copulations, in which females have simple vaginas. (C) Long-tailed Duck (Clangula hyemalis), and (D) Mallard (Anas platyrhynchos), two species with a long phallus and high levels of forced copulations, in which females have very elaborate vaginas (size bars = 2 cm). ] = Phallus, * = Testis, star = Muscular base of the male phallus, > = upper and lower limits of the vagina (From: Brennan et al. 2007).

Eversion of a male Muscovy duck penis

Explosive eversion and functional morphology of the duck penis -- Coevolution of male and female genitalia in waterfowl has been hypothesized to occur through sexual conflict. This hypothesis raises questions about the functional morphology of the waterfowl penis and the mechanics of copulation in waterfowl. Brennan et al. (2010) used high-speed video of phallus eversion and histology to describe for the first time the functional morphology of the avian penis. Eversion of the 20 cm muscovy duck penis is explosive, taking an average of 0.36 sec, and achieving a maximum velocity of 1.6 m sec−1. The collagen matrix of the penis is very thin and not arranged in an axial-orthogonal array, resulting in a penis that is flexible when erect. To test the hypothesis that female genital novelties make intromission difficult during forced copulations, Brennan et al. (2010) investigated penile eversion into glass tubes that presented different mechanical challenges to eversion. Eversion occurred successfully in a straight tube and a counterclockwise spiral tube that matched the chirality of the waterfowl penis, but eversion was significantly less successful into glass tubes with a clockwise spiral or a 135° bend, which mimicked female vaginal geometry. These results support the hypothesis that duck vaginal complexity functions to exclude the penis during forced copulations, and coevolved with the waterfowl penis via antagonistic sexual conflict.

Near the junction of the vagina and shell gland of female birds are
deep glands lined with simple columnar epithelium. These are the sperm
storage tubules, so called because they can store sperm for long periods
of time (10 days to 2 weeks). After an egg is laid, some of these sperm
may move out of the tubules into the lumen of the tract, then migrate farther
up to fertilize another egg.

King et al. (2002) found that spermatozoa from two different inseminations (one with stained sperm, one with unstained sperm) generally
segregated into different storage tubules in both chicken and turkey hens. Storage tubules contained mixed populations of spermatozoa were
found in only 4% of chicken and 12% of turkey storage tubules examined. They concluded that the mechanism of last-male precedence does
not appear to be due to the stratification of spermatozoa within the tubules.

Innervation of sperm storage tubules (Freedman et al. 2001) -- Immunohistochemical staining of a turkey uterovaginal junction and sperm storage tubules. This micrograph shows a fluorescing neuron (green) near some sperm storage tubules (SST). The blue areas (se) are the surface epithelium lining the lumen of the uterovaginal junction and the epithelium of the sperm storage tubules. The arrow points to a magenta-stained area of one SST that indicates the presence of actin (a protein found in smooth muscle. The total image is 19 micrometers across.

This association between neurons and SSTs provides evidence that SSTs are innervated and suggests that the storage and release of sperm from SSTs can, perhaps, be controlled.

Post-insemination events (Birkhead and Brillard 2007) -- Most birds do not have a phallus and, in these species, insemination occurs via the so-called ‘cloacal kiss.’ Depending on taxa, sperm are ejaculated into the cloaca or vagina and rely on their motility to reach the numerous sperm-storage tubules (SSTs) located at the junction of the vagina and the uterus. As a consequence of selection during their migration through the vagina, only 1–2% of inseminated sperm enter the SSTs, the rest are probably ejected the next time that the female defecates. The SSTs contain only morphologically normal sperm, suggesting either that only normal sperm successfully traverse the vagina or that only normal sperm are ‘accepted’ by the SSTs. An unknown but probably small proportion of sperm move directly to the infundibulum (the site of fertilization) without entering the SSTs, although these are likely to fertilize only a single ovum.

That sperm in the SSTs are invariably positioned with their heads directed towards the distal end of the tubule suggests that egress from the SSTs is passive. Sperm are lost from the SSTs more or less continuously at a constant per capita rate. They enter the uterus and are carried passively to the infundibulum. Sperm accumulate or move relatively slowly through the infundibulum so that there is usually a population available to fertilize each ovum as it is ovulated. On ovulation, the ovum is captured by the prehensile, funnel-shaped infundibulum and the sperm swarm over the surface of the ovum; their target is the germinal disc, which contains the female pronucleus. At this stage, the ovum is bounded by the inner perivitelline layers (IPVL). The clustering of sperm and holes made by sperm in the IPVL around the germinal disc suggest that sperm might use chemical signals to locate the germinal disc.

In contrast to most other taxa, where only a single sperm enters the ovum, polyspermy is typical in birds. Several sperm enter the germinal disc region, hydrolyzing the IPVL via the acrosome reaction of the sperm, whereby the release of enzymes from the sperm acrosome enables the sperm nucleus to enter the ovum. However, only a single spermatozoon fuses with the female pronucleus and the remaining sperm are shifted to the periphery of the germinal disc and play no further part in development. Fertilization includes the penetration of ovum by sperm as well as the fusion of the male and female pronuclei (syngamy). Because embryo development begins almost immediately, many cell divisions have occurred by the time the ovum has become incorporated into the egg and the egg is laid (in most species) 24 hr later.

Repelling clingy exes helps snipe save sperm --
Writer Gore Vidal once said that he never passed up an opportunity to have
sex or appear on television. Some male birds would disagree on at least
one count. Having mated with a female, a male Great Snipe (Gallinago
media) will reject her further advances and even chase her away. Male
Great Snipe form leks to eye up the talent before choosing a mate. A few
males get the most sex. Popular birds can get more than half of the matings,
perhaps 10 a day. Hence their pickiness, suggest Saether et al. (2001).
As male Great Snipe take no part in caring for their offspring, it was
thought they had nothing to lose by mating as much as possible. But top
males, overburdened with potential partners, must share sperm with care
and spread their favors around. Sperm budgeting is the only possible explanation
for male snipes' ungrateful behavior. Like a nightclub, Great Snipe
leks see their share of aggravation. "All four kinds of mating conflicts
happen" - male choice, female choice, and male and female competition -
explains Saether. Males are more likely to repel clingy exes if there are
a lot of other females around. Females fight with one another, and males
from neighboring territories chase their rivals' females away. Hostility
towards old flames might be a bid to maintain order. "If a male gets rid
of an unwanted female it's one less problem to worry about," says Saether.
Female snipe probably seek to mate again so that they can get enough sperm
to fertilize their eggs. Rejected females tend to lower their sights and
settle for less popular males. -- John
Whitfield, Nature Science Update

Birds' eggs, like the birds themselves, vary enormously in size. The
largest egg from a living bird belongs to the ostrich. It is over
2000 times larger than the smallest egg produced by a hummingbird (see
photo to the right; Source: http://www.pma.edmonton.ab.ca/vexhibit/eggs/vexhome/sizeshap.htm).
Ostrich eggs are about 180 mm long and 140 mm wide and weigh 1.2 kg. Hummingbird
eggs are 13 mm long and 8 mm wide and they weigh only half of a gram. The
extinct Elephant Bird from Madagascar produced an egg 7 times larger than
that of the Ostrich! Within the egg, three extraembryonic membranes support
the life & growth of the embryo:

amnion

surrounds only the embryo

inner layer of cells secretes amniotic fluid in which the embryo floats;
fluid keeps the embryo from drying out and protects it

grows larger as embryo grows, fuses with the chorion & is called the
chorio-allantoic membrane

works together with chorion to permit respiration (exchange of oxygen and
carbon dioxide) and excretion

important in storage of nitrogenous wastes (uric acid)

Relative egg mass (corrected for adult mass) is greater in species with longer embryonic periods (days) among 64 passerine species in tropical Venezuela, subtropical Argentina, and north temperate Arizona. Open symbols reflect cavity-nesting species and show an interacting effect where their larger clutches are associated with relatively smaller eggs.

Egg size variation among tropical and temperate songbirds -- Species with “slow” life history strategies (long life, low fecundity) are thought to produce high-quality offspring by investing in larger, but fewer, young. Larger eggs are indeed associated with fewer eggs across taxa and can yield higher-quality offspring. Tropical passerines appear to follow theory because they commonly exhibit slow life history strategies and produce larger, but fewer, eggs compared with northern species. Martin (2008) found that relative egg mass (corrected for adult mass) varies extensively in the tropics and subtropics for the same clutch size, and proposed a hypothesis to explain egg size variation both within the tropics and between latitudes: Relative egg mass increases in species with cooler egg temperatures and longer embryonic periods to offset associated increases in energetic requirements of embryos. Egg temperatures of birds are determined by parental incubation behavior and are often cooler among tropical passerines because of reduced parental attentiveness of eggs. Cooler egg temperatures and longer embryonic periods explained the enigmatic variation in egg mass within and among regions, based on field studies in tropical Venezuela (36 species), subtropical Argentina (16 species), and north temperate Arizona (20 species). Alternative explanations were not supported. Thus, large egg sizes may reflect compensation for increased energetic requirements of cool egg temperatures and long embryonic periods that result from reduced parental attentiveness in tropical birds.

Egg composition and hatchling phenotype -- Parental
investment in eggs and, consequently, in offspring can profoundly influence
the phenotype, survival and evolutionary fitness of an organism. Avian
eggs are excellent model systems to examine maternal allocation of energy
translated through egg size variation. Dzialowski1and Sotherland (2004)
used the natural range in Emu (Dromaius novaehollandiae) egg size,
from 400 g to >700 g, to examine the influence of maternal investment in
eggs on the morphology and physiology of hatchlings. Female Emus provisioned
larger eggs with a greater absolute amount of energy, nutrients and water
in the yolk and albumen. Variation in maternal investment was reflected
in differences in hatchling size, which increased isometrically with egg
size. Egg size also influenced the physiology of developing Emu embryos,
such that late-term embryonic metabolic rate was positively correlated
with egg size and embryos developing in larger eggs consumed more yolk
during development. Large eggs produced hatchlings that were both heavier
(yolk-free wet and dry mass) and structurally larger (tibiotarsus and culmen
lengths) than hatchlings emerging from smaller eggs. As with many other
precocial birds, larger hatchlings also contained more water, which was
reflected in a greater blood volume. Emu maternal investment in offspring,
measured by egg size and composition, is significantly correlated with
the morphology and physiology of hatchlings and, in turn, may influence
the success of these organisms during the first days of the juvenile stage.

the yolk is suspended in the center of the egg by twisted strands of protein
fibers called chalazae (shown below)

Yolk contains maternal antibodies -- Antibodies
are deposited in eggs during yolk formation through the deposition of immunoglobulins,
primarily IgY (also called IgG), in the yolk. In Chickens (Gallus domesticus),
maternal IgY is catabolized by offspring over the first 14 days post-hatching
and, by about 5 days post-hatching, offspring begin to synthesize their
own IgY. As a result, after approximately two weeks the circulating IgY
in young is principally of endogenous origin. Adult levels are attained
between six weeks and six months of age. However, maternal antibodies may
continue to affect offspring phenotype even after they are catabolized
by influencing growth and developmental rates. In the absence of maternal
IgY in chickens (due to surgical bursectomy of the mother during her own
embryogenesis), the number of cells in the spleen that help lymphocytes
(helper T cells) attack antigens (foreign proteins on pathogens) is depressed.
Also, the immune responsiveness of offspring is depressed, which could
lower the survival of offspring particularly in harsh disease environments
(Grindstaff et al. 2003).

Maternal secretion of antibodies and absorption by the young occur only prenatally in birds (with the exception of pigeon crop milk)
(From: Boulinier and Staszewski 2008).

The familiar color of a chicken’s egg yolk (a) is in stark
contrast to the richly pigmented egg yolk of a lesser Black-backed Gull, Larus
fuscus (b). Such high maternal investment of carotenoids into egg yolk
is typical among wild bird species, suggesting that these biologically
active pigments serve important functions in the developing bird
(From: Blount et al. 2000).

Why egg yolk is yellow (or red) (Blount et al.
2000) -- Egg yolk in birds is colored yellowish-red by carotenoids. Until
recently, there has been no adaptive explanation of why many egg-laying
animals provision their eggs so richly with carotenoids. It now appears
that, in developing birds, carotenoids protect vulnerable tissues against
damage caused by free radicals. Athough embryonic tissues depend on oxidizable,
unsaturated fatty acids in yolk, their abundance makes the tissues susceptible
to peroxidation caused by reactive oxidative metabolites and by free radicals,
which are produced as normal by-products of metabolism. Protection against
lipid peroxidation in young birds is afforded by the actions of yolk-derived
carotenoids and other antioxidants, like vitamin E. Antioxidants also protect
passively-acquired antibodies (IgY; see above) against break-down. Thus,
maternal investment in egg composition, including carotenoids, might have
a greater influence on offspring viability than has been realized. The
use of carotenoid pigments in the sexual displays of female birds might
indicate their ability to produce high quality eggs and chicks.

albumen

90% water & 10% protein

the embryo's water supply, but also serves as a 'shock-absorber' to help
protect the embryo

buffers embryo from sudden changes in temperature

shell membranes

attached to the shell are two membranes, the inner and outer shell membranes.
They protect the egg from bacterial invasion and help prevent rapid evaporation
of moisture from the egg.

Keratin fibers from the outer shell membrane can be seen
above, attached to thecalcium carbonate crystals that make up the main shell
structure.(Source: http://www.rit.edu/~tld0898/SEM.html)

Weaker
Birds Use Steroids to Boost Offspring -- Verboven et al. (2003)
reported that female gulls in poor condition were more likely to give their
chicks a hormone boost to improve their chances of survival. Verboven and
her colleagues experimentally enhanced maternal condition by supplementary
feeding Lesser
Black-backed Gulls (Larus fuscus) during egg formation and compared
the concentrations of steroids (including testosterone) in their eggs with
those in eggs laid by control females. Egg androgens could affect offspring
performance directly through chick development and/or indirectly through
changes in the competitive ability of a chick relative to its siblings.
Contrary to expectation, females with experimentally enhanced body condition
laid eggs with lower levels of androgens. This suggests that less healthy
females pass on more steroids than healthy ones in a bid to enhance the
performance of their young. Verboven noted that “We originally thought
that gulls in good condition would put more steroids in their eggs. But
we discovered that healthy birds don’t tend to give their eggs the extra
boost.” She compared the situation to struggling athletes who take performance-enhancing
drugs. She added: “A poor sports person maybe wants to use steroids to
conceal poor performance but if you are good you don’t need to use them.”

Avian mothers create different phenotypes by hormone deposition in their eggs -- In birds, mothers deposit substantial amounts of androgens in their eggs, and experimental evidence indicates that these maternal androgens influence the chick's early development. Despite the well-known organizing role of sex steroids on brain and behavior, studies on avian maternal egg hormones almost exclusively focus on the chick phase. Eising et al. (2005) found that, in Black-headed Gulls, maternal androgens in the egg enhance the development of the nuptial plumage and the frequency of aggressive and sexual displays (see Figure above) almost 1 year after hatching.
The long-lasting effects may be mediated by an upregulation of androgen receptors later in life. Alternatively, the
early hormone exposure may have influenced the hypothalamus-pituitary-gonad axis, resulting in higher
androgen production later in life.
The long-lasting effects of egg androgens are almost certainly
beneficial for Darwinian fitness. Successful territory establishment
and defense by means of aggressive interactions are essential for
reproductive success in this colonial breeder. In addition, the
displays are important for mate selection.
Clearly, in birds, maternal hormone deposition in eggs may profoundly influence individual differentiation of fitness related
traits. Since these hormones suppress early immune function of the chick and reduce long-term survival, mothers may be faced with a trade-off between producing offspring with lower survival prospects but higher reproductive success per year, or with higher chances of survival and lower annual reproductive output. By producing eggs that differ in levels of maternal hormones, mothers seem to produce a variety of phenotypes, perhaps an adaptive strategy in unpredictable environmental conditions. Since natural selection acts upon such phenotypic variation, shaping a population's demography, the role of maternal androgens in this selective process may be much greater than anticipated until now.

Egg colors and markings have strong adaptive values. Originally, birds'
eggs were probably all white, as reptile eggs are. Eggs that are laid on
the ground or in open nests in trees, rather than in cavities, often exhibit
cryptic coloration. The eggs blend in with their surroundings and are much
less visible to potential predators (e.g., a Killdeer
nest).

Sometimes eggs that are laid in open nests are white at first. They
then become stained by the mud and rotting vegetation in the nest. Grebes
lay white eggs that become stained and cryptically colored over time.

In some species, such as the Common Murre, where different females lay
eggs with very different markings, the uniqueness may have a purpose. Distinctive
patterns, as in the eggs shown below, help females identify their own egg
in a colony where thousands
of eggs may dot a cliff face.

Eggs of kingfishers and other cavity nesting birds, such as woodpeckers
and some owls, are often white. The brightness of the eggs may help the
parents to more easily locate them in the cavity. Shown here is the egg
of a Barn Owl.

Evolution of egg color and patterning in birds -- Avian eggs differ so much in their color and patterning from species to species that any attempt to account for this diversity might initially seem doomed to failure. Kilner (2006) reviewed the literature that, when combined with the results of some comparative analyses, suggests that just a few selective agents can explain much of the variation in egg appearance. Ancestrally, bird eggs were probably white and immaculate. Ancient diversification in nest location, and hence in the clutch's vulnerability to attack by predators, can explain basic differences between bird families in egg appearance. The ancestral white egg has been retained by species whose nests are safe from attack by predators, while those that have moved to a more vulnerable nest site are now more likely to lay brown eggs, covered in speckles, just as Wallace hypothesized more than a century ago. Even blue eggs might be cryptic in a subset of nests built in vegetation. It is possible that some species have subsequently turned these ancient adaptations to new functions, for example to signal female quality, to protect eggs from damaging solar radiation, or to add structural strength to shells when calcium is in short supply. The threat of predation, together with the use of varying nest sites, appears to have increased the diversity of egg coloring seen among species within families, and among clutches within species. Brood parasites and their hosts have probably secondarily influenced the diversity of egg appearance. Each drives the evolution of the other's egg color and patterning, as hosts attempt to avoid exploitation by rejecting odd-looking eggs from their nests, and parasites attempt to outwit their hosts by laying eggs that will escape detection. This co-evolutionary arms race has increased variation in egg appearance both within and between species, in parasites and in hosts, sometimes resulting in the evolution of egg color polymorphisms. It has also reduced variation in egg appearance within host clutches, although the benefit thus gained by hosts is not clear.

Many small songbirds have eggs with just a ‘ring’ of small spots around the broad end that does little to make the eggs cryptic. Evidence now suggests that such spots are located where the eggshell is a bit thinner (likely due to a calcium deficiency in the diet of female birds), with the pigment serving to strengthen the shell (Gosler et al. 2005). The spots consist of protoporphyrin pigment that birds synthesize during production of the heme component of hemoglobin (Burley and Vadhera 1989) and integration of this pigment into the eggshell provides additional strength. When a female bird has insufficient calcium to deposit in a shell, protoporphyrin molecules that have a semi-crystalline structure similar to that of eggshells are apparently deposited instead instead of calcium. As a result, the spots occur precisely where the shell is a bit thinner.

Several species of birds have blue eggs, and David Lack (1958) suggested that, in habitats where light levels are low, blue eggs might be cryptic. If true, that could help explain the blue eggs of some open-cup nesting birds that occur in forest habitats such as Wood Thrushes. However, Lack’s hypothesis cannot explain why some birds that nest in cavities, like European Starlings and Eastern Bluebirds, also have blue eggs. One hypothesis is that the blue-green color of eggshells represents a signal of female quality to their mates ( Moreno and Osorno 2003). The pigment responsible for the blue-green color is biliverdin, a substance produced when the hemoglobin of damaged red blood cells is catabolized and also known to have strong antioxidant properties. Antioxidants are important because they can convert free radicals, molecules that can damage DNA, proteins, and other macromolecules, into less reactive substances. Deposition of this pigment in eggshells by laying females may, therefore, signal their capacity to produce antioxidants and control free radicals. Male birds paired to females of such quality that they are able to deposit antioxidants in eggshells rather than retaining them may then expend greater effort in caring for their superior offspring (Kilner 2006). In support of this hypothesis, the provisioning rates of male Pied Flycatchers (Ficedula hypoleuca) and the intensity of the blue coloration of eggs were found to be positively correlated (Moreno et al. 2004). Also, female Eastern Bluebirds in better body condition were found to lay more colorful eggs, supporting the hypothesis that biliverdin pigmentation in eggshells reflects female condition (Siefferman et al. 2006).

Egg-laying:

"Initially the female stood motionless in the nest cup. The first sign of approaching egg- laying was usually intensified breathing, occasionally with rhythmic opening and closing of the bill that pointed either horizontally forwards or more or less upwards. The head was drawn in and the body feathers were somewhat fluffed out; the Coal Tit in addition raised its crown feathers. The tail was kept horizontal or elevated up to about 45 degrees”. Then the tip of the tail started nodding movements synchronously with rhythmic depressions of the rump.These movements which apparently were caused by throes of parturition when the egg traveled down the oviduct, were almost invisible to begin with but gathered in strength and ended with a sudden elevation of the rump that marked the moment of egg-laying. Then the bird “froze” in a motionless posture, termed “recovery phase.” This last rise of the rump clearly indicated that the egg had just been laid.

Duration of egg-laying varies a great deal even within species. The opening and closing of the bill and rhythmic movements of the back and tip of the tail occurs repeatedly for up to 4 minutes in the Prairie Warbler, presumably corresponding to the duration of egg- laying. For 3 eggs of the Goldcrest, only 8-9 seconds elapsed between the first visible sign of pressure and the moment of egg- laying. In tits, this period varied from about 10 to 77 seconds, mostlv 20-30 seconds. The Cuckoo (Cuculus canorth) which is a brood parasite, is known to lay the egg remarkably swift, usually within 10 seconds with a lower limit of only 3-4 seconds. Presumably this short duration is an adaptation to its parasitic behavior."--- From: Haftorn (1996).

Female birds turns part of the cloaca and the last segment of the oviduct
inside out ("like a glove"). The vent is then everted and the egg emerges
far outside at the end of the bulge. As a result, the egg does not contact
the walls of the cloaca and get contaminated by feces. In addition, the
intestine and inner part of the cloaca are kept shut by the emerging egg,
and their contents cannot leave when the hen strains to deliver the egg.
Therefore, eggs are always clean when laid (van der Molen 2002).